Status and distribution of the Endangered javanicus birmanicus in : a conservation tragedy

M iguel P edrono,HaMinhT uan,Philippe C houteau and F r E´ d E´ ric V allejo

Abstract From January 2005 to December 2007 field been at least an 80% reduction in the global banteng range surveys were conducted in the Central Highlands region since the 1980s (IUCN, 2008). Only seven populations with of Vietnam to assess the status of banteng Bos javanicus . 50 banteng are known to remain in its native range: birmanicus. The population of banteng was estimated to be four in Java, two in Thailand and one in Cambodia. No 74–103. It has declined by at least 50% since the mid- population in the natural range exceeds 500 individuals 1990s and the is likely to go extinct in Vietnam in (Phanthavong & Santiapillai, 1991; Srikosamatara & Sutee- the near future. Remaining herds are small, although re- thorn, 1995; Soriyun, 2001). As a consequence, the banteng cruitment still exists. Large portions of the species’ range in is categorized as Endangered on the IUCN Red List (IUCN, the early 1990s are no longer occupied and the maximum 2008). Three subspecies of banteng are recognized, al- area of occupancy of the species in Vietnam is c. 2,670 km2. though further research is required to verify the Only five disconnected populations persist. The most im- of this wild species (Byers et al., 1995). The Java portant are in Yok Don National Park (30–44 individuals) banteng Bos javanicus javanicus is confined to a few pro- and Ea So Nature Reserve (23–31). However, our surveys tected areas on the islands of Java and Bali, the Borneo suggest that these populations are exposed to risks of banteng Bos javanicus lowi to the island of Borneo, and disease outbreak and will only be viable if there is active scattered, small populations of the Burma banteng Bos management to facilitate recovery. Interviews carried out at javanicus birmanicus persist in Myanmar, China, Thailand, the survey sites indicate that the status of banteng in Malaysia, Cambodia, Lao and Vietnam. The Burma ban- Vietnam is determined by commercial poaching in response teng has been extirpated in India, Bangladesh, Brunei to demand for trophies. Future conservation actions need to Darussalam and Peninsular Malaysia; it is considered the target poor governance, the root cause of banteng decline, most threatened of the three subspecies (Heinen & Sriko- which precludes effective management of protected areas in samatara, 1996). There is also a large non-native population Vietnam and places several species of large at risk of Java banteng in northern Australia, representing a po- of extinction nationally. tentially important reservoir for the native populations of 2006 Keywords Bos javanicus birmanicus, , this subspecies (Bradshaw et al., ). distribution, poaching, protected areas, Vietnam The banteng is probably the ancestor of South-east Asian domestic cattle and its extinction would represent a major loss of genetic material for improving domestic cattle breeds. Successful banteng conservation remains Introduction elusive because the same forces that caused the probable 1980 1990 nce widely distributed in South-east Asia, the banteng extinction of the Bos sauveli in the sor s 2007 OBos javanicus is now restricted to small fragmented are still operating (Hedges et al., ). External anthro- populations. The number of individuals remaining in its pogenic threats and intrinsic biological traits (e.g. low native range is estimated to be 3,000–5,000 and there has population densities, large home-range requirements and low reproduction rates; Cardillo et al., 2005) are driving

MIGUEL PEDRONO (Corresponding author) CIRAD, Campus International de banteng populations to extinction. But the underlying cause Baillarguet, 34398 Montpellier Cedex 5, France, Wild Cattle Conservation of banteng decline in South-east Asia is the growth of the Project, National Institute of Husbandry, Thuy Phuong, Tu Liem, 2004 Hanoi, Vietnam, and CIRAD Representative Office, 3rd Floor, 35, Dien Bien human population (Sodhi et al., ). Impacts of human Phu Street, Hanoi, Vietnam. E-mail [email protected] population density on biodiversity conservation have been 2003 HA MINH TUAN Wild Cattle Conservation Project, National Institute of demonstrated for several animal taxa (McKee et al., ). Animal Husbandry, Hanoi, Vietnam. High human population densities lead to an increase in PHILIPPE CHOUTEAU Institute of Zoology, Chinese Academy of Sciences, human pressure on ecosystems and undermine conserva- Beijing, China. tion activities. As a consequence, South-east Asia has ex- FRE´DE´RIC VALLEJO CIRAD, Campus International de Baillarguet, Montpel- perienced one of the highest rates of population lier, France, and Wild Cattle Conservation Project, National Institute of 2002 Animal Husbandry, Hanoi, Vietnam. extinctions (Ceballos & Ehrlich, ). In Vietnam the Received 11 March 2008. Revision requested 13 May 2008. situation is particularly critical, with the highest human Accepted 28 July 2008. population density in South-east Asia and a rapidly expanding

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market economy. Vietnam experienced considerable changes extensive degradation. Moreover, because of the influx of in human density and land-use patterns after the North–South settlers from northern Vietnam much of the original forest Vietnam War, and old-growth forests were lost at a rate of cover of the Central Highlands has been cleared to make way 1 14.6%yearÀ over 2000–2005 (Koh, 2007). This has resulted in for settlements, plantations and agriculture. large-scale fragmentation and has rendered banteng more vulnerable to poaching. Large-scale internal transmi- Methods gration towards the Central Highlands occurred after the war (Dak Lak People’s Committee, 1994)andofficialre- Survey areas were chosen based on both historical records settlement programmes have increased human density in and interviews with local villagers. Surveys were carried out the areas of most suitable banteng habitat. A large portion from January 2005 to December 2007, mainly in the dry of the banteng range in Vietnam is now subject to extreme season (October–June) when field access is possible. Sur- levels of human disturbance and intervention. veys were conducted on foot, motorcycle and, in Yok Don A survey of banteng is a priority action for large mammal National Park, by elephant, both during the day and night. researchers in Vietnam (Duckworth & Hedges, 1998). Un- We searched for all species of wild cattle (B. javanicus, derstanding the current status of banteng populations in Bos gaurus and wild arnee) with the this densely populated country may help predict any future exception of the Pseudoryx nghetinhensis,whichgener- declines in the species’ range and focus conservation efforts ally occurs in more rocky areas. At least two surveys were on the populations most at risk. Here we present information conducted per site, and the data collected at each site were gathered during a study of the distribution and status of all pooled, with the assumption that there was no significant wild cattle in Vietnam over 3 years. We report our findings change in population during the study period. The number of for banteng by comparing the current distribution with surveyors was 3–8, including field rangers and local guides. that of 10–15 years ago (Duckworth & Hedges, 1998) and The survey team was generally split into 2–3 groups operating summarize the factors that have determined the current simultaneously in different parts of the surveyed areas. There precarious status of banteng in Vietnam. was at least one experienced observer in each group. The extremely low density of banteng in Vietnam pre- Study area cludes the use of line transect surveys. The most practical way of estimating banteng distribution and abundance was The surveyed area covered 10 provinces in the Central to search for signs of activity, especially tracks and dung, in Highlands region of Vietnam where banteng were known likely areas. Searches focused on salt licks, open grasslands, to have occurred in the early 1990s. This region can broadly wetland margins, watercourses, ridges and large mammal be divided into three geographical zones: (1) the Kotum trails. Coordinates of only fresh tracks and dung (, 1 week Plateau and southern Annamite mountains in the north, (2) old) were recorded. Banteng tracks are on average narrower the flat central plateau of Gia Lai and Dak Lak, and (3) the than gaur tracks (Wharton, 1957; Prayurasiddhi, 1997). In Da Lat Plateau and southern mountains. These areas have a some cases, however, the assignment of tracks to banteng or subtropical monsoon climate. The south-west monsoon winds gaur was not possible, and in such circumstances they were of June–November bring rains and occasional typhoons to not recorded. Although there is no notable difference the eastern slopes of the mountains. In December–April between dung of banteng and gaur, the presence of tracks there is a drier period that is characterized by winds of near the dung was used to pre-identify the species of origin. the north-east monsoon. The survey focused on Yok Don Dung samples were then stored in both alcohol and 2 2 National Park (1,155 km ), Ea So Nature Reserve (220 km ), RNALater, a stabilization reagent, for later analysis. Species 2 Cat Tien National Park (719 km ), Vinh Cuu Nature Reserve assignment was based on the analysis of a cytochrome b gene 2 (538 km ) and several state forest enterprises. fragment with several species-specific diagnostic nucleotides The vegetation of the Central Highlands consists primarily (Rivie`re-Dobigny et al., 2009). The fragment sequenced of lowland deciduous dipterocarp forest dominated by Dip- corresponds to positions 867–1140 in the cytochrome b gene terocarpus obtusifolius, Dipterocarpus tuberculatus, Shorea of domestic cattle Bos taurus. DNA amplifications were obtusa and Shorea siamensis, and highland evergreen forest performed using the following primers: L15612: 59-CGA- characterized by Lagerstroemia calyculata, Shorea cochinchi- TCA-ATY-CCY-AAY-AAA-CTA-GG-39 and H15915 nensis and Anisoptera scaphula. Bamboos such as Bambusa (reverse): -TCT-CCA-TTT-CTG-GTT-TAC-AAG-AC-39 balcooa are common in the evergreen forest, particularly as (Hassanin et al., 2006). Although banteng sometimes forage colonizers of open areas after disturbance. Few patches of in the same grazing areas as domestic cattle (i.e. in Ea So primary forest remain because of extensive selective logging Nature Reserve, Vinh Cuu Nature Reserve and Krong Trai and forest replacement by plantations. This region also Nature Reserve) and produce similar-sized and shaped suffered from the spraying of defoliants during the North– tracks, the molecular approach we used facilitated unam- South Vietnam War (Stellman et al., 2003), resulting in biguous identification. Such an approach proved to be more

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effective than camera trapping, which was abandoned early Gia Map, the banteng is now locally extinct, although it was in the study. still present there in the early 1990s (Fig. 1, Table 1). Local This molecular approach was not, however, effective for villagers told us that banteng were present until the early genotyping field samples to allow the minimum population 1990s in all these sites but that they were poached to size and sex ratio to be determined. Amplification success extinction within the last decade. We estimate the species’ rate of microsatellites from faecal DNA was low. High area of occupancy (sensu IUCN, 2008) in Vietnam to be 2 2 temperatures in central Vietnam seem to negatively affect c. 2,670 km in total, with c. 1,433 km in Dak Lak Province, 2 2 the conservation of microsatellites before the dung is c. 431 km in Gia Lai Province, c. 228 km in Phu Yen Prov- 2 collected (Wehausen et al., 2004). It was also not possible ince and c. 578 km on the border between Binh Phuoc and to estimate population sizes from dung density because of Dong Nai provinces. All these areas appear to be encroached difficulties in estimating defecation and dung decay rates by human activities. There is no evidence that banteng (Wiles, 1980). Thus, we used the difference in size of tracks survive in other provinces (Table 1). Extirpation of herds has that allowed identification of individuals when the herd resulted in the loss of at least 52% of the 1990s range of the was small. It was difficult, however, to estimate population species in Vietnam. Three populations are inside protected size for large herds using this approach. In such cases the areas (Yok Don National Park, Ea So and Krong Trai Nature population size reported was therefore based on direct Reserves) and two outside (Chu Prong and Dong Phu observations, mainly from forest rangers and local villagers districts), and c. 82% of the total number of individuals (i.e. former or present hunters). occur within a protected area and 18% outside. Banteng were also occasionally observed by our survey We estimate that the total number of banteng in Vietnam teams, largely opportunistically and during the day. Noc- is 74–103 (Table 1), with no population . 50; the last turnal watches were occasionally carried out in places population of this size occurred in Yok Don National Park, where abundant activity signs were recorded during the which previously comprised a smaller Yok Don National day but successful observations were few, presumably be- Park and Ea Sup District, until the early 1990s. Yok Don is cause of the shy behaviour of banteng (caused by high levels still the largest population of banteng in Vietnam but it 2 of human disturbance and poaching). However, such high has declined to 30–44, surviving over an area of c. 1,155 km . levels of human presence offered opportunities for fruitful The second largest population is in Ea So Nature Reserve, interviews with local people (all the herds of banteng that where we estimate that 23–31 banteng survive in an area of c. 2 were recorded from tracks had been observed several times 278 km . The populations of Chu Prong District, Krong Trai by local people). We interviewed local villagers and forest Nature Reserve and Dong Phu District have been reduced officials about the past and current occurrence of banteng. to a few individuals (Table 1). Calves or juveniles are present Semi-structured discussions focused on banteng and herd in all five remaining populations, indicating that some re- numbers, locations and dates of observations, threats and cruitment still exists. poaching rates. Some questions were worded differently The populations of banteng in Vietnam have suffered and repeated to cross-check answers, especially those con- major declines, essentially because of poaching. A large cerning the size of specific herds. Illustrations were pro- number of banteng have been poached for commercial duced at the end of the interviews to confirm species’ purposes since the mid 1990s and poaching shows no signs identities when confusion existed between descriptions of of abating. We documented the deaths of 13 individuals banteng and gaur. trophies of wild cattle were also during 2002–2006, including 11 in protected areas (Table 2). examined whenever possible. Duckworth & Hedges (1998), This is a minimum estimate; local villagers and officials from who used survey reports and articles, complemented by the Forest Protection Department are often reluctant to interviews with local people and government staff, to assess report poaching of large mammals such as banteng. Poaching the status of banteng in Indo-China, were our source for is for trophies, comprising the head and/or horns, which are data on historical banteng populations. sold for c. USD 900. Other body parts do not appear to be sold. Demand from wealthy Vietnamese living in urban areas Results drives poaching. Poachers use cable snares or guns. Army personnel stationed at the border between Vietnam and The banteng range in Vietnam now extends from Chu Cambodia (i.e. in Yok Don National Park and Chu Prong Prong District in the north to Vinh Cuu Nature Reserve in District) also poach for subsistence food needs. The number the south (Fig. 1). Banteng were documented at six of the 18 of herds lost has been similar across provinces and habitat localities surveyed. These localities represent five discon- types, although intensive poaching is particularly severe nected populations (Chu Prong, Yok Don, Ea So, Krong where the largest populations of banteng still exist (Table 2). Trai and Dong Phu), separated by highly modified areas. In In all the areas surveyed, including protected areas, we Chu Mom Ray, Dak R’Lap, Nam Nung, Ta Dung, Bu Dang, recorded other human activities, such as fishing, wood–resin Nam Cat Tien, Bi Doup Nui Ba, Cat Loc, Nui Ong and Bu exploitation, wood cutting, forest fires, shifting cultivation

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FIG. 1 Current and past range of banteng in Vietnam. Numbers indicate named sites in Table 1. The rectangle on the inset indicates the location of the main figure in Vietnam.

and livestock grazing. In Ea So, Yok Don, Krong Trai and creasing in Chu Prong and Dong Phu districts, leading to Vinh Cuu the grasslands are generally exploited by banteng loss of habitat and . Road construction during the night and by domestic cattle during the day. The is affecting all the places surveyed by encouraging human number of domestic cattle around Ea So Nature Reserve has settlement and thereby increasing human pressures. approximately doubled in the last 5 years and most are severely affected by both foot-and-mouth disease and bovine Discussion pasteurellosis. The management board of Ea So Nature Reserve is even breeding its own herd of 115 domestic cattle In the 1960s banteng were still widespread in central Vietnam inside the Reserve for economic profit. The rate of forest but intensively hunted (Wharton, 1968). In 1990–1993 the clearing by migrants from northern Vietnam is also in- total population in Vietnam was estimated to be 200–300

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TABLE 1 Previous (Duckworth & Hedges, 1998) and current estimates (this study) of banteng populations at 18 locations inVietnam. Numbered locations refer to Fig. 1. Survey-hours Habitat Previous status Status or in Location1 Province area (km2) or estimate estimate in 2005–20072 2005–2007 1, Chu Mom Ray NP Kon Tum 566 Present (early 1990s) Extinct 17.5 2, Chu Prong District Gia Lai 431 Present 7–12, 1 herd 22.0 3, Ea Sup/north Yok Don NP Dak Lak 573 70–90 (1995) 13–19, 2–3 herds 98.0 4, South Yok Don NP Dak Lak 582 35–45 (1993) 17–25, 3–4 herds 166.5 5, Ea So NR Dak Lak 278 .17 (1997) 23–31, 4–6 herds 154.0 6, Dak R’Lap District Dak Nong 57 8 (1993) Extinct 21.0 7, Krong Trai NR Phu Yen 228 15–20 (1997) 8–10, 2 herds 32.0 8, Nam Nung NR Dak Nong 108 Present (1993) Extinct 19.2 9, Ta Dung NR Dak Nong 214 Present (early 1990s) Extinct 38.5 10, Bu Gia Map NP Binh Phuoc 223 Present (early 1990s) Extinct 110.0 11, Dong Phu District Binh Phuoc 40 Present 6, 1 herd 89.5 12, Bu Dang District Binh Phuoc 48 Present (early 1990s) Extinct 32.0 13, Nam Cat Tien/Cat Dong Nai 383 Present (1998) Extinct 458.0 Tien NP 14, Vinh Cuu NR Dong Nai 538 Present Same herd as location 11 230.6 15, Bi Doup Nui Ba NP Lam Dong 640 Present (early 1990s) Extinct 10.5 16, Cat Loc/Cat Tien NP Lam Dong 306 Present (1995) Extinct 182.5 17, Ninh Son District Ninh Thuan 26 40–45 (1998) Extinct 8.0 18, Nui Ong NR Binh Thuan 370 10 (1994) Extinct 12.8

1These 18 localities represent 16 distinct populations (north–south Yok Don NP and Dong Phu District–Vinh Cuu NR each constitute single populations). NP, National Park; NR, Nature Reserve. 2Minimum and maximum population sizes were estimated when it was not possible to determine the exact number of individuals; the values are the mean minimum and maximum population sizes from all the surveys in the particular area

(Le, 1995). An estimate in 1998 derived from interviews dropped to levels so low that local villagers and our suggested that the population was no more than 170–195 survey team failed to encounter any individuals. None of individuals, with a strong ongoing decline (Do & Le, the five remaining populations will be able to survive 1998). Our estimate for 2004–2007 is yet lower (74–103), without management to facilitate recovery. persisting in a few areas of lower human pressures as The average herd size of five that we observed during the small widely dispersed herds. This population has expe- dry season is similar to the herd size reported for this rienced a decline in number of . 50% since the mid species in densely vegetated areas, which is typically , 8 1990s. Eleven of the 16 populations that were probably (Halder, 1973, 1976). However, herd size was expected to be still present in the mid 1990s are now extinct or have higher than this average figure in areas such as Yok Don

TABLE 2 Reported banteng deaths during 2002–2006 in Vietnam based on interviews with forest rangers and national press releases. Numbered locations refer to Fig. 1. Year Location* Main habitat type Details 2002 7, Krong Trai NR Semi-evergreen forest 1 adult caught by a snare 2002 11, Dong Phu District Semi-evergreen forest 1 juvenile caught by a snare 2003 5, Ea So NR Dry dipterocarp forest 1 adult shot 2004 3, North Yok Don NP Dry dipterocarp forest 1 adult caught by a snare 2004 5, Ea So NR Dry dipterocarp forest 1 adult caught by a snare 2005 4, South Yok Don NP Dry dipterocarp forest 1 adult shot 2005 5, Ea So NR Dry dipterocarp forest 2 adults caught by a snare 2006 2, Chu Prong District Dry dipterocarp forest 1 trophy of banteng seized 2006 3, North Yok Don NP Dry dipterocarp forest 1 juvenile found dead 2006 5, Ea So NR Dry dipterocarp forest 1 trophy of banteng seized 2006 7, Krong Trai NR Semi-evergreen forest 2 adults caught by snares

*NP, National Park; NR, Natural Reserve

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National Park or Ea So Nature Reserve where the vegeta- Management policies of various government bodies are tion is dominated by open dry dipterocarp forests with often incompatible with the objectives of protected areas. extensive grasslands (Wharton, 1957, 1968). It is unlikely This includes the construction of roads and dams in Ea So that estimates would be much higher during the rainy sea- and Krong Trai Nature Reserves, and Yok Don and Bu Gia son when herds of banteng typically aggregate (Wharton, Map National Parks. Many protected areas are too small to 1968; Srikosamatara & Steethorn, 1995) because of the small sustain large mammal populations or too heavily degraded number of herds. Sympatric populations of gaur live in to satisfy conservation goals (Tordoff et al., 2004). Such all the locations where banteng are still extant in Vietnam. small areas do not always include the wet and dry season Although at a national level gaur largely outnumber banteng, ranges necessary to sustain a viable population of banteng. banteng are more abundant in the open dry dipterocarp All these issues are compounded by the prevailing view of forests of Yok Don and Ea So protected areas, probably government officials who regard ethnic minority commu- because of habitat preferences. nities as a problem for conservation rather than as potential Local villagers did not report any sudden declines in conservationists (Sheil & Lawrence, 2004). Moreover, few banteng populations since the mid 1990s that could have rangers come from local ethnic minorities; most are from been attributed to disease outbreaks. More likely, intense northern Vietnam and have no practical field experience poaching pressure has depleted or extirpated populations. (McElwee, 2000, 2002). If poaching pressures remain high, the species is likely to go We recommend enforcement of the legislation on extinct in Vietnam; the Yok Don population is likely to be wildlife hunting and trading in Vietnam to stem poaching the last to survive because of its larger size and connection of banteng. Recognizing this problem is the first step to with other populations. Forest clearing can benefit banteng addressing it (Smith & Walpole, 2005). It is essential that as it provides additional grazing, and we found that motivated rangers patrol protected areas to deter poachers banteng tend to move into open areas to feed at night. and destroy snares. Incentive systems rewarding anti- Thus, patterns of shifting cultivation and the associated poaching activities should be implemented, and it may be formation of secondary forest in South-east Asia have his- better to have fewer well-paid and capable rangers than torically provided banteng with suitable habitat (Wharton, many low-paid ones. Local people’s concerns should not 1968; Sodhi & Brook, 2006). be ignored in the development of future protected area Even though the banteng is legally protected in Vietnam policies; ethnic minorities and Kinh (the dominant ethnic little attention is paid to the implementation of wildlife group) rangers need to cooperate to protect wildlife protection laws, and traffic in banteng and gaur trophies is (Steinmetz et al., 2006). The presence of domestic cattle common (Nguyen, 2009). Such trophies, which are thought at many banteng grazing sites poses a risk of transmission to bring luck to the owners, can be found for sale in shops and outbreak of infectious disease in banteng. The vacci- and are exhibited in many houses, hotels and restaurants nation of domestic cattle in the periphery of protected areas without any apparent threat of prosecution. Smugglers are against foot-and-mouth disease and bovine pasteurellosis aware that any fines imposed will be outweighed by the would be a short-term measure to avoid an epizooty in financial rewards and that growing economic wealth in banteng. Livestock fences could be used to confine domes- urban areas is fuelling demand. tic cattle outside certain protected areas to avoid such Although the direct cause of the collapse of banteng epizooties and to preclude genetic introgression and for- populations in the sites surveyed is poaching, the un- aging competition. Such fences, built by the Wild Cattle derlying factor that allows poaching to continue unabated Conservation Project on 4.3 km of the border of Cat Tien is poor governance, as has already been reported in National Park, have already limited contact between the Vietnam (Kemp et al., 1997) and elsewhere (Smith et al., herds of gaur inside the Park and adjacent domestic cattle. 2003). Nearly all the herds of banteng in Vietnam reside Conservation efforts for the banteng in Vietnam should inside protected areas (Table 1) but most of these are not prioritize Yok Don National Park, the largest protected managed in practice, despite high protected area staff- area of Vietnam, which supports the main population of 2 ing levels (e.g. one ranger per 7.7 and 5.6 km in Yok Don banteng in extensive dry dipterocarp forest containing and Cat Tien National Parks, respecively). During c. 1,703 seasonal pools, the optimal habitat for wild cattle. To the survey-hours over 3 years we never met any ranger patrols west, Yok Don National Park borders Srepok Wilderness in the protected areas surveyed. The protected areas that Area in Cambodia. This has the largest population of wild we surveyed appear to be ‘paper parks’, with inadequate cattle in the Indo-Chinese Peninsula (Desai & Vuthy, 1996), and unmotivated staff on low government pay scales, with the potential to repopulate Yok Don National Park tacitly accepted corruption of officials and high political with banteng, gaur and . That banteng patronage. As a consequence, no part of the banteng’s move across the Vietnam-Cambodia border can explain extent of occurrence in Vietnam is effectively protected why other recent surveys of banteng in Yok Don National from poaching. Park report much lower population size estimates (Nguyen,

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